Zuo et al. BMC Cancer (2021) 21:505 https://doi.org/10.1186/s12885-021-08223-7

RESEARCH ARTICLE Open Access Artificial pneumothorax improves radiofrequency of pulmonary metastases of close to mediastinum Taiyang Zuo1,2†, Wenli Lin1†, Fengyong Liu1,2 and Jinshun Xu1,2,3*

Abstract Background: To investigate the feasibility, safety and efficacy of percutaneous (RFA) of pulmonary metastases from hepatocellular carcinoma (HCC) contiguous with the mediastinum using the artificial pneumothorax technique. Method: A total of 40 lesions in 32 patients with pulmonary metastases from HCC contiguous with the mediastinum accepted RFA treatment from August 2014 to May 2018 via the artificial pneumothorax technique. After ablation, clinical outcomes were followed up by contrast enhanced CT. Technical success, local tumor progression (LTP), intrapulmonary distant recurrence (IDR), and adverse events were evaluated. Overall survival (OS) and local tumor progression free survival (LTPFS) were recorded for each patient. Results: The tumor size was 1.4 ± 0.6 cm in diameter. RFA procedures were all successfully performed without intra- ablative complications. Technical success was noted in 100% of the patients. Five cases of LTP and 8 cases of IDR occurred following the secondary RFA for treatment. Slight pain was reported in all patients. No major complications were observed. The 1, 2, and 3-year LTPFS rates were 90.6, 81.2, and 71.8%, and the 1, 2, and 3-year OS rates were 100, 100 and 87.5%, respectively. Conclusion: Artificial pneumothorax adjuvant RFA is a feasible, safe, and efficient method for treatment of pulmonary metastases from HCC contiguous with the mediastinum. Keywords: Lung , Artificial pneumothorax, Mediastinum, Radiofrequency ablation, Hepatocellular carcinoma

Background However, the minimal invasive thermal technique re- Image-guided percutaneous local ablation has been mains challenging for treatment of pulmonary metastasis widely used for the treatment of pulmonary metastasis, abutting the mediastinum, as a result of the proximity to based on the high capability on accurate orientation of the or . In 2007, Iguchi et al. reported that needles and real-time visualization of targets [1–5]. the primary technical effectiveness of radiofrequency ab- lation (RFA) was only 43% at 6 months postablation for * Correspondence: [email protected] treatment of 15 lung tumors contiguous with mediasti- †Taiyang Zuo and Wenli Lin contributed equally to this work. num [6]. Subsequently, studies on the efficacious im- 1 Department of , Jinan Central Hospital Affiliated to provement of RFA for treatment of lung tumors Shandong University, Jinan 250013, Shandong, China 2Department of , Department of Interventional contiguous with mediastinum were rarely reported be- Ultrasound, Chinese PLA General Hospital, Beijing 100853, Shandong, China cause of the insurmountable technique risk. Therefore, a Full list of author information is available at the end of the article

© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zuo et al. BMC Cancer (2021) 21:505 Page 2 of 8

safe and effective adjuvant method should be developed The exclusion criteria were: I) patients with severe to reduce the risk of puncture and ablation for improve- coagulation dysfunction including thrombocyte num- ment of RFA efficiency of lung tumor contiguous with ber < 30 × 10 [9]/L, international normalized ratio mediastinum. (INR) > 3.0, prothrombin time > 30 s, or prothrombin Artificial pneumothorax is a standard technique that activity (PTA) < 40%; II) acute infection or chronic in- serves as an effective adjuvant for the clinical ablation fection in acute phase; III) severe pulmonary hyper- of peripheral lung tumors [7, 8], which could be used tension defined as mean pressure for separation between the punctured needle path and (mPAP) > 35 mmHg measured by cardiac normal tissues after gas administration into the catheterization and (or) Doppler echocardiogram; IV) pleural cavity [9]. It is suggested that the pulmonary severe pulmonary insufficiency defined as PaO2 <60 tumors could be accurately separated from medias- mmHg, with and without PaCO2 >50mmHg; and V) tinal structures during an artificial pneumothorax pro- implantation of cardiac pacemaker. cedure. In that case, thermal damage to heart, aorta, or main nerves would be controlled, and pain caused Artificial pneumothorax adjuvant RFA procedure by pleura heat could be effectively alleviated. In All patients underwent contrast enhanced CT (CECT) addition, the heat-sink effect of RFA could be reduced of the chest prior to RFA in order to evaluate the as well due to the artificial-induced space between tu- anatomic relationship between lesions and peripheral mors and vessels [10]. Therefore, this strategy could cardiovascular structures. CECT was performed using not only significantly reduce the risks of puncture the SOMATOM Force CT system (Siemens, Munich, and ablation, but also enhance RFA efficiency for Germany) with intravenous administration of Omni- complete ablation. Compared with the air administra- paque (GE Medical, USA) as a contrast agent. Before tion to form artificial pneumothorax [9], CO2 is less the procedure, patients in a supine position received common but displays good properties including high continuous electrocardiogram (ECG) monitoring and diffusion coefficient, inert reaction to RFA, and pure were hypodermically injected with 1% . Then, gas injection without unidentified substance [11]. the puncture point and needle track were determined Therefore, we investigate the feasibility, safety and ef- by CT scan (MIYABI, Siemens, Munich, Germany). ficacy of using artificial CO2 pneumothorax in this Subsequently, the biopsy needle was penetrated into study for mediating RFA of pulmonary metastases the target in a direction away from the heart and ves- contiguous with the mediastinum. sels. When the procedure was accomplished, the bi- opsy needle was removed. Methods Thereafter, the artificial pneumothorax technique was Patients enrollment performed using a 22-G puncture needle (NPAS-100, This study was approved by the institutional ethics COOK, USA) with a blunt tip. The needle was inserted committee of our hospital, patients diagnosed with along the well-designed puncture proposal, which speci- pulmonary metastases contiguous with the mediasti- fies insertion route, depth and angle. When the needle num who underwent RFA were retrospectively inves- tip reached the edge of the pleura, the needle core was tigated at our hospital from August 2014 to May pulled out, 1–2 ml of saline was injected locally to form 2018. The target lesions of all cases were confirmed a water capsule using T-stopcock and tubes. Then, saline clinically or pathologically as hepatocellular carcin- in the tube flowed into the cavity, and the water capsule oma (HCC). “Contiguous with mediastinum” was de- disappeared gradually as the needle tip continued to be fined as the distance between metastatic lesion and inserted and reached into the pleura cavity. Then, 100– mediastinum was less than 3 mm on CT or MR 500 ml of CO2 gas was frequently administered to separ- images. ate the lung parenchyma. CT scanning was performed The inclusion criteria for this study were: I) a single individually after injection of 100, 200, 300, 400, and metastatic lesion contiguous with mediastinum in the 500 ml CO2 until the tumor was separated from the unilateral lobe of lung; II) lesion size less than 3 cm mediastinum and a feasible puncture path was in diameter; III) orthotopic HCC shown to be inactive established. without recurrence and intrahepatic metastasis as in- After the RF electrode was successfully inserted into dicated by enhance imaging after surgical and (or) the tumor based on the CT scanning assessment, percu- interventional therapy; IV) no increase in numbers of taneous RFA (Model 1500, RITA Medical System, pulmonary lesions after 1–2 months of observation; Mountain View, CA, USA) was performed at 60–70 W V) patients refuse to accept surgical resection; and for 5–12 min at a rating temperature of 90 °C. During VI) Karnofsky performance status (KPS) greater than the process, an 18-G unipolar electrode (Uniblate) was 70%. chosen (the length of the needle was 15 cm and the Zuo et al. BMC Cancer (2021) 21:505 Page 3 of 8

maximum ablation range of a single electrode was 3 × 3 definition of major complication included moderate AE, cm2). The ablation procedure was terminated when the severe AE, life-threatening or disabling event, patient ablation zone completely overlapped the target tumor death or unexpected pregnancy abortion. Mild AE was and an ablative margin of 5–10 mm beyond the tumor defined as minor complication. To assess the post- boarder was achieved. Then, the RF electrode was ablative pain, a visual analogue scale (VAS, a numerical withdrawn for coagulation of the needle track to avoid rating scale: 0–10) was used based on previous publica- needle implantation and bleeding. During the procedure, tions: score 1–3 corresponding to slight pain, score 4–6 5–10 mg of morphine was intravenously injected for an- corresponding to moderate pain and score 7–10 corre- algesia and sedation based on pain degree of patients. sponding to severe pain [5, 15]. The ablation zone was defined as the pulmonary texture around the tumor that showed a circular exudation Statistical analysis shadow with ground-glass appearance on CT imaging. Statistical analysis was performed using SPSS software After RFA, CO2 in the pleura cavity was aspirated with a (version 22.0; SPSS Inc., Chicago, IL, USA). Categorical 50-ml syringe and expelled through the T-stopcock until variables were described as numbers (percentages). Con- no additional gas could be aspirated. tinuous variables were described as mean ± standard de- viation (SD) or medians (range) according to the Follow up normality results using the Kolmogorov–Smirnov test. CECT was performed to evaluate the therapeutic re- Survival was calculated by Kaplan-Meier survival sponse of tumors at 1, 3, 6, and 12 months post abla- analysis. tion and at 6-month intervals thereafter. If incomplete tumor ablation was detected by CECT, secondary Results RFA was performed. According to the reporting cri- Patients characteristics teria of image-guided tumor ablation [12, 13], tech- The graphical diagram of this study is shown in Fig. 1.A nical success was defined as a tumor that was treated total of 32 patients with 40 pulmonary metastatic tu- according to the initial protocol and was covered mors contiguous with the mediastinum were confirmed completely by the ablation zone. Local tumor progres- from HCC using biopsy and then accept RFA treatment sion (LTP) was defined as the appearance of new during this study. Prior to RFA treatment, no other tumor foci at the ablative margin. Intrapulmonary dis- treatment options were performed in all patients. As tant recurrence (IDR) was defined as any occurrence shown in Tables 1, 62.5% (20/32) of patients were males, of a new tumor foci in the lung. and 37.5% (12/32) of patients were females. The median During follow-up, adverse events (AEs) after ablation, age was 61 years old, ranging from 44 to 72 years old. local tumor progression free survival (LTPFS), and over- The mean tumor diameter was 1.4 ± 0.6 cm with a me- all survival (OS) were recorded for each patient. AEs dian distance of 0.1 cm from the mediastinum, ranging were classified in this study according to AE classifica- from 0 to 0.3 cm. 87.5% (28/32) patients had cirrhosis, tion of the Society of Interventional Radiology [14]. The mainly due to viral hepatitis B or C (96.4%). In total,

Fig. 1 Graphical diagram of this study. KPS: Karnofsky performance status; LTP: local tumor progression; IDR: intrapulmonary distant recurrence; LTPFS: local tumor progression-free survival; OS: overall survival Zuo et al. BMC Cancer (2021) 21:505 Page 4 of 8

Table 1 Characteristics of the 32 patients with 40 pulmonary patients with LTP and IDR and technical success was metastatic tumors contiguous with the mediastinum obtained on CECT imaging assessment. The 1, 2, 3-year Characteristics Values, n (%) LTPFS rates after RFA were 90.6, 81.2, and 71.8%, and Age (y), median (range) 61 (44–72) OS rates of 1, 2 and 3 years were 100, 100 and 87.5%, re- Sex spectively (Fig. 3). Male 20 (62.5) Female 12 (37.5) Complications Pulmonary metastatic tumors (cm) No major complications were observed during and fol- lowing RFA procedure, such as severe pneumothorax, Tumor diameter (mean ± SD) 1.4 ± 0.6 aeroembolism, hemothorax, lung abscess, alveolar bleed- – Distance from mediastinum, median (range) 0.1 (0 0.3) ing, and tumor seeding. No AEs were relevant to the Comorbidity proximity of tumors to the mediastinum, such as vagus/ Cirrhosis 28 (87.5) recurrent laryngeal/phrenic nerve injury, vessel or 12 (37.5) oesophageal injury, pericardial effusion, , and Diabetes 10 (31.2) cardiac infraction. The overall complication rate was 100% in the 32 patients with 40 tumors. All of them Cardiovascular disease 6 (18.7) were minor complications including slight pain of VAS Intrahepatic diseases score 1–3(n = 32), asymptomatic pneumothorax (n = Viral hepatitis B 20 (62.5) 10), asymptomatic pleural effusion (n = 4), transient Viral hepatitis C 7 (21.9) postablation syndrome of low-grade fever (n = 12) and Alcohol 2 (6.2) general malaise (n = 16), as shown in Table 2. All com- – Others 3 (9.4) plications resolved after 1 2 days postablation without any treatment. Child-Pugh class A 18 (56.2) B 14 (43.7) Discussion Artificial pneumothorax was first reported by Francini a Laboratory data (mean ± SD) century ago to treat pulmonary tuberculosis [16]. By AFP (ng/ml) 88.7 ± 67.2 injecting nitrogen between the parietal and visceral Total bilirubin (μmol/l) 19.1 ± 8.4 pleura, tuberculosis progression was suppressed by the Albumin (g/l) 35.2 ± 6.7 reduction of blood flow and lymphatic reflux after pul- Prothrombin time (%) 80.4 ± 18.3 monary compression. During the past decades and en- Platelet count (10^9/l) 156 ± 48 lightened by this report, artificial pneumothorax has been successfully performed for protection of chest wall Creatinine (mmol/l) 6.5 ± 3.2 [17], relief of chest pain [18], and biopsy of pulmonary – MELD score, median (range) 12 (6 22) or mediastinal tumors [19]. AFP alpha fetal protein, MELD model for end-stage liver disease, SD In this study, the technique of artificial pneumothorax standard deviation was first validated as a feasible, safe, and efficient adju- vant method for RFA upon treatment of pulmonary me- 56.2% (18/32) of patients were characterized as Child- tastases contiguous with the mediastinum. As shown in Pugh classification A, and 43.7% (14/32) of patients were the results, technique success of RFA was 100% (32/32) characterized as Child-Pugh classification B. The median without major complications under artificial pneumo- model for end-stage liver disease (MELD) score was 12 thorax intervention, and the 1, 2, 3-year LTPFS rates with range between 6 and 22. were 90.6 and 81.2%, and 71.8%, respectively, resulting in the valid treatment efficiency and effective protection Therapeutic outcomes of proximate mediastinal structures. Compared to 43% RFA technical success was achieved in all patients after only of the primary technical effectiveness reported by the average 267.5 ± 94.4 ml administration of CO2 was Iguchi et al, these results were comparable to the overall performed in each case. One of the most representative technique efficacy of standard RFA of lung intraparench- cases was presented in Fig. 2a-l. During the median ymal tumors away from mediastinum [20, 21]. In gen- follow-up of 29 months (ranging from 12 to 57 months), eral, our findings indicated that the use of artificial LTP occurred in 15.6% (5/32) of patients and IDR oc- pneumothorax had safe and efficient local control for curred in 25% (8/32) of patients (Table 2). Subsequently, CT-guided RFA of lung metastasis contiguous with the the secondary RFA treatment were performed for the mediastinum. Zuo et al. BMC Cancer (2021) 21:505 Page 5 of 8

Fig. 2 Artificial pneumothorax adjuvant RFA of pulmonary metastases contiguous to the mediastinum (a 67-year-old man with a metastatic lesion in the superior lobe forepart of right lung). Tumor size, 1.5 × 1.2 cm. a Before ablation, chest CT imaging was performed to evaluate the anatomic relationship between tumor and peripheral cardiovascular structures. b Subsequently, a 22-G needle tip was used to create a puncture that reached the outer edge of pleura for injection of 1–2 ml saline. c The needle tip entered into the pleura, and the saline in the tube flowed

into the cavity. d-e CO2 gas was administered gradually with a syringe until the tumor was separated from the mediastinum. f CT image during RFA showed the electrode inserted into the tumor and located away from the mediastinum by proxy of artificial pneumothorax. g The ablation zone gradually increased following the RFA procedure. h After RFA, the pulmonary texture around tumor showed a circular exudation shadow with ground-glass appearance on CT image. i Contrast enhanced CT image 1 month after RFA showed no enhancement of the ablated tumor contiguous to the mediastinum. j-l The size of ablated tumor decreased gradually after RFA during follow up at 3, 6, and 12 months, respectively

Given that 18-G needles are commonly used for gas In comparison with the air used before, the adminis- administration in thorax, a potential complication for tration of CO2 to produce artificial pneumothorax in that procedure is mainly iatrogenic pneumothorax [8, 9, this study could be adsorbed more quickly by blood and 22, 23]. To avoid damage to visceral pleura or pulmon- reduce the risks of air embolism and injuries to normal ary parenchyma, we used a 22-G blunt needle with nega- tissues [24]. As a result, the blood oxygen saturations in tive pressure during the procedure and withdrew CO2 all of the 32 patients were not influenced based on the gas from the plural space after ablation. As a result, per- ECG monitoring. sistent pneumothorax or pleural hemorrhage with a However, excessive CO2 in the pleural cavity can chest tube drainage did not occurred. cause several adverse effects, including a) decrease in Zuo et al. BMC Cancer (2021) 21:505 Page 6 of 8

Table 2 RFA Outcomes of pulmonary metastases contiguous patients with pulmonary metastasis, inoperability and with the mediastinum (n = 32) intolerance are commonly coexisted because of old Values, n (%) age, comorbidity, and operative suffering sentiment. Follow up (months), median (range) 29 (12–57) Therefore, radiotherapy is the most common option Technical success 32 (100) for the treatment of pulmonary metastasis contigu- ous with mediastinum. Unfortunately, only 63% of 2- Local tumor progression (LTP) 5 (15.6) year OS rate was reported after 327 inoperable pul- Intrapulmonary distant recurrence (IDR) 8 (25) monary oligometastases treated with stereotactic Major complications 0 body radiotherapy (SBRT) [26]. Comparatively, Wah Minor complications et al. reported that the estimated OS rates at 1 and Slight pain 32 (100) 3 years were 96.7 and 74.7%, respectively, after 60 Asymptomatic pneumothorax 10 (31.2) colorectal pulmonary oligometastases treated by RFA [27]. To the treatment of extrahepatic oligmetastases Asymptomatic pleural effusion 4 (12.5) from HCC, Zhao et al. have reported that the 1-, 2- Low-grade fever 12 (37.5) year OS rates were 91 and 70%, respectively [28]. General malaise 16 (50) Consistent with these results, 1-, 2-, 3-year OS rates of 100, 100 and 87.5% were found in this study for the pulmonary oligometastases contiguous with mediastinum, attributing to the benefits of artificial returned blood volume, increase in central venous pneumothorax adjuvant technique. pressure, and decrease in blood pressure; and b) im- Of note, the technique is non-indicated in some paired respiratory function and results in dyspnea, cases, including patients suffering from pleural adhe- especially in the patients with poor pulmonary func- sion or severe respiratory insufficiency. Limitations tions [25]. Furthermore, when excessive compression on this study was related to the fact that only 32 pa- of lung parenchyma changes the electrical conductiv- tients with 40 tumors were subjected to this method, ity and heat conduction of RF, the ablation efficiency owning to the focus is on the metastatic tumors will be influenced, resulting in the damage enlarge- from HCC. Further studies should explore the artifi- ment of lung tissues [9]. Therefore, it is preferable cial pneumothorax procedure as an adjuvant for RFA to minimize the amount of CO2 injection during the to understand the full extent of clinical benefits. process of artificial pneumothorax. Compared to the previously reported injection volume of 400–1400 ml [22], the 100–500 ml of injected CO2 in this study Conclusion was more efficient to establish a safe puncture path CT-guided RFA after artificially pneumothorax is a between the tumor and mediastinum. safe and effective method for the treatment of pul- As known, resection is preferred for the treatment monary metastases contiguous with the mediastinum. of pulmonary tumors, especially for the lesions con- More samples should be examined to confirm the tiguous with mediastinum. However, as to the present results.

Fig. 3 Overall survival (OS) and local tumor progression-free survival (LTPFS) curves during patient follow-up Zuo et al. BMC Cancer (2021) 21:505 Page 7 of 8

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